Viruses that infect marine cyanobacteria (cyanophages) are dsDNA tailed viruses belonging to the Caudovirales. A number of distinct genera infect the cyanobacteria including T7-like podoviruses, T4-like myoviruses, lambdoid siphoviruses and TIM5-like myoviruses that we recently discovered in the Red Sea. These cyanophages are considered to be a key force influencing host abundance, diversity and evolution. In order to understand their impact we need to assess cyanophage abundance, composition and distribution patterns. Using the plaque assay with 3 Synechococcus and 3 Prochlorococcus hosts, we found that cyanophage abundance and relative composition varied greatly with host strain. We further found viral-genus and host-dependent differences in the breadth of virus host range. These findings have important implications for host-virus interactions in the oceans. However, such differences prevent us from achieving accurate measures of total cyanophage abundances and from gaining insights into their impacts on hosts. To overcome these limitations and to gain the ability to quantify all cyanophages belonging to a particular viral genus, we adapted the solid-phase single-molecule PCR polony method for this purpose using degenerate primers for viral genus-specific signature genes. This culture-independent method revealed that cyanophages are highly abundant in the Red Sea, dramatically more so than inferred from estimates based on culture-dependent methods. Furthermore, it revealed drastic differences in the abundance of different cyanophage types in the Red Sea. Such measurements will be of paramount importance for assessing virus population dynamics and for gaining understanding into the impact of different viral types on their hosts and on ecosystem functioning.